Redox Control of Chemotrophic Sulfur Oxidation of Paracoccus pantotrophus

Abstract

The reaction cycle of the reconstituted Sox enzyme system of Paracoccus pantotrophus requires the periplasmic proteins SoxYZ, SoxXA, SoxB, and SoxCD. The heme enzyme SoxXA covalently binds the sulfur substrate to the thiol of the single cysteine residue of SoxY located at its carboxy-terminal end. Bound sulfur is then oxidized to sulfate by a series of reactions. These involve sulfur dehydrogenase SoxCD which oxidizes the protein-bound sulfane sulfur to sulfone in a unique six-electron transfer. Bound sulfone is then hydrolyzed off by the sulfate thiohydrolase SoxB to regenerate SoxYZ. The flavoprotein SoxF enhances the rate of sulfur oxidation in vivo as evident from mutant analysis and we have specified its action in vitro. SoxYZ unlike the other Sox proteins is inactivated upon reduction. When the Sox system is reconstituted with inactivated SoxYZ, the thiosulfate-oxidizing activity is drastically decreased. SoxF reverses this inactivation and may mediate a conformational change of SoxYZ possibly by a transient interprotein disulfide. The membrane protein SoxV and the thioredoxin SoxS are essential for chemotrophic growth as evident from homogenote mutants defective in these proteins. Evidence is presented that both proteins transfer reductant from the cytoplasm to the periplasm and that SoxYZ is the final target of this transfer to balance the redox state of the Sox enzyme system or reduce a SoxY .. Y interprotein disulfide.

Identification of two inactive forms of the central sulfur cycle protein SoxYZ of Paracoccus pantotrophus

“…Homogeneous SoxF has a sulfide dehydrogenase activity in vitro [17]. This activity, however, is not considered to be of relevance in vivo since P. pantotrophus harbors three different sulfide-oxidizing activities [18] and SoxF affects the thiosulfate metabolism [16]. Moreover, SoxF does not function in sulfur oxidation in vitro in the Sox enzyme system as reconstituted from homogeneous active Sox proteins.…”

Thiosulfate-Dependent Chemolithoautotrophic Growth of Bradyrhizobium japonicum

“…A survey of the B. japonicum USDA110 genome revealed multiple homologues of sox genes; however, it was not clear if these homologues were functional for the oxidation of inorganic sulfur compounds and chemolithotrophic growth in this bacterium (7). The sox gene cluster in P. pantotrophus GB17 comprises at least 15 genes, soxTRSVWXYZABCDEFGH, which are responsible for thiosulfate oxidation and chemolithotrophic growth (9).…”

SoxAX Binding Protein, a Novel Component of the Thiosulfate-Oxidizing Multienzyme System in the Green Sulfur Bacterium Chlorobium tepidum

“…Thiosulfate is one of the most-abundant forms of reduced sulfur in nature, and the ability to oxidize this compound is distributed over many microorganisms across different phyla (6,7,14,19,21,43). It sometimes occurs that some members within a phylum can utilize thiosulfate while others cannot.…”

“…From the direct sequencing of the sox genes, as well as from the results of current whole-genome-sequencing projects, genes predicted to be involved in inorganic sulfur metabolism have been identified in a variety of microorganisms, including many of the genes encoding Sox proteins (soxA, soxB, soxF, soxX, soxY, and soxW) that occur in a cluster as in P. pantotrophus (19,21,22). In the green sulfur bacterium C. limicola f. thiosulfatophilum, Verté et al (60) reported that sox genes occur in a similar cluster.…”